Stravinsky had begun work on the opera in 1908, but put it aside for several years after he had received the commission from Sergei Diaghilev for the ballet The Firebird. He completed it in 1914, after he had completed his other two major ballets for Diaghilev, Petrushka and The Rite of Spring. Because the time between the writing of the first and second acts extended over six years, stylistically the work reflects Stravinsky's significantly changed approach to composition, and this can clearly be detected when performances are given. Stravinsky subsequently turned aside from large productions to concentrate on chamber music and the piano.

After its founding in 1956, The Santa Fe Opera in Santa Fe, New Mexico presented many operas by Stravinsky during its first decade, including—during its opening season in 1957—The Rake's Progress. Additionally, several performances of The Nightingale, with Stravinsky himself conducting in 1962 were part of his 80th birthday celebrations; other stagings took place in 1963, 1969, 1970, and 1973.[2]

In 2014, the opera was paired with Mozart's The Impresario (Der Schauspieldirektor) for a new production given by the Santa Fe company in which the action took place in Paris in the 1920s.[3] The cast included Anthony Michaels-Moore, Brenda Rae, Meredith Arwady, and Erin Morley.[4]

At the seashore just before sunrise, a Fisherman hears the song of the Nightingale, which causes him to forget his troubles. The Cook has brought officials from the court of the Emperor to hear the Nightingale, telling of the beauty of its singing. However, the Nightingale is nowhere to be heard. The Court Chamberlain promises the Cook a position as private cook to the Emperor, if she can find the Nightingale, who finally appears, and receives an invitation from the Cook and the Chamberlain to sing for the Emperor. The Nightingale accepts the invitation, but says that its sweetest song is in the forest.

Courtiers festoon the palace with lanterns in advance of the singing of the Nightingale. The Cook describes the Nightingale to the courtiers noting that it is small, gray and virtually invisible, but its song causes its listeners to cry. A procession denotes the Emperor's arrival. He commands the Nightingale to sing, and its singing touches him so deeply that he offers the bird a reward of a golden slipper to wear about its neck. Later, three Japanese emissaries offer the Emperor a mechanical nightingale, which begins to sing. The genuine bird flies away, and the angry emperor orders it banished from his realm. He names the mechanical bird "first singer".

The Emperor is ill and near death; the figure of Death appears in the Emperor's chamber. The ghosts of the Emperor's past deeds visit him. while he calls for his court musicians, but the genuine nightingale has reappeared, in defiance of the imperial edict, and has begun to sing. Death hears the Nightingale's song and is greatly moved, and asks it to continue, which it does on condition that Death returns to the emperor his crown, sword and standard. Death assents and gradually removes himself from the scene as the Nightingale continues to sing. The Emperor slowly regains his strength, and on seeing the Nightingale, offers it the "first singer" post at court. The Nightingale says that it is satisfied with the Emperor's tears as reward, and promises to sing for him each night from dusk until dawn.